Evolutionary genomics of inversions in Drosophila pseudoobscura: Evidence for epistasis

Stephen Wade Schaeffer, M. Paula Goetting-Minesky, Miro Kovacevic, John R. Peoples, Jennifer L. Graybill, Jonathan M. Miller, Kyungsun Kim, Julie G. Nelson, Wyatt W. Anderson

Research output: Contribution to journalArticle

83 Citations (Scopus)

Abstract

Drosophila pseudoobscura harbors a rich polymorphism for paracentric inversions on the third chromosome, and the clines in the inversion frequencies across the southwestern United States indicate that strong natural selection operates on them. Isogenic inversion strains were made from isofemale lines collected from four localities, and eight molecular markers were mapped on the third chromosome. Nucleotide diversity was measured for these loci and formed the basis of an evolutionary genomic analysis. The loci were differentiated among inversions. The inversions did not show significant differences among populations, however, likely the result of extensive gene flow among populations. Some loci had significant reductions in nucleotide diversity within inversions compared with interspecies divergence, suggesting that these loci are near inversion breakpoints or are near targets of directional selection. Linkage disequilibrium (LD) levels tended to decrease with distance between loci, indicating that some genetic exchange occurs among gene arrangements despite the presence of inversions. In some cases, however, adjacent genes had low levels of interlocus LD and loosely linked genes had high levels of interlocus LD, suggesting strong epistatic selection. Our results support the hypothesis that the inversions of D. pseudoobscura have emerged as suppressors of recombination to maintain positive epistatic relationships among loci within gene arrangements that developed as the species adapted to a heterogeneous environment.

Original languageEnglish (US)
Pages (from-to)8319-8324
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume100
Issue number14
DOIs
StatePublished - Jul 8 2003

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Linkage Disequilibrium
Genomics
Drosophila
Gene Order
Nucleotides
Chromosomes
Southwestern United States
Gene Flow
Genetic Selection
Genetic Recombination
Population
Genes

All Science Journal Classification (ASJC) codes

  • General

Cite this

Schaeffer, Stephen Wade ; Goetting-Minesky, M. Paula ; Kovacevic, Miro ; Peoples, John R. ; Graybill, Jennifer L. ; Miller, Jonathan M. ; Kim, Kyungsun ; Nelson, Julie G. ; Anderson, Wyatt W. / Evolutionary genomics of inversions in Drosophila pseudoobscura : Evidence for epistasis. In: Proceedings of the National Academy of Sciences of the United States of America. 2003 ; Vol. 100, No. 14. pp. 8319-8324.
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Schaeffer, SW, Goetting-Minesky, MP, Kovacevic, M, Peoples, JR, Graybill, JL, Miller, JM, Kim, K, Nelson, JG & Anderson, WW 2003, 'Evolutionary genomics of inversions in Drosophila pseudoobscura: Evidence for epistasis', Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8319-8324. https://doi.org/10.1073/pnas.1432900100

Evolutionary genomics of inversions in Drosophila pseudoobscura : Evidence for epistasis. / Schaeffer, Stephen Wade; Goetting-Minesky, M. Paula; Kovacevic, Miro; Peoples, John R.; Graybill, Jennifer L.; Miller, Jonathan M.; Kim, Kyungsun; Nelson, Julie G.; Anderson, Wyatt W.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 100, No. 14, 08.07.2003, p. 8319-8324.

Research output: Contribution to journalArticle

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AU - Schaeffer, Stephen Wade

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AU - Peoples, John R.

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N2 - Drosophila pseudoobscura harbors a rich polymorphism for paracentric inversions on the third chromosome, and the clines in the inversion frequencies across the southwestern United States indicate that strong natural selection operates on them. Isogenic inversion strains were made from isofemale lines collected from four localities, and eight molecular markers were mapped on the third chromosome. Nucleotide diversity was measured for these loci and formed the basis of an evolutionary genomic analysis. The loci were differentiated among inversions. The inversions did not show significant differences among populations, however, likely the result of extensive gene flow among populations. Some loci had significant reductions in nucleotide diversity within inversions compared with interspecies divergence, suggesting that these loci are near inversion breakpoints or are near targets of directional selection. Linkage disequilibrium (LD) levels tended to decrease with distance between loci, indicating that some genetic exchange occurs among gene arrangements despite the presence of inversions. In some cases, however, adjacent genes had low levels of interlocus LD and loosely linked genes had high levels of interlocus LD, suggesting strong epistatic selection. Our results support the hypothesis that the inversions of D. pseudoobscura have emerged as suppressors of recombination to maintain positive epistatic relationships among loci within gene arrangements that developed as the species adapted to a heterogeneous environment.

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